Robust and distributed neural representation of action values

  1. Eun Ju Shin
  2. Yunsil Jang
  3. Soyoun Kim
  4. Hoseok Kim
  5. Xinying Cai
  6. Hyunjung Lee
  7. Jung Hoon Sul
  8. Sung-Hyun Lee
  9. Yeonseung Chung
  10. Daeyeol Lee  Is a corresponding author
  11. Min Whan Jung  Is a corresponding author
  1. Korea Advanced Institute of Science and Technology, Republic of Korea
  2. Institute for Basic Science, Republic of Korea
  3. Karolinska Institutet, Sweden
  4. New York University Shanghai, China
  5. Kyungpook National University School of Medicine, Republic of Korea
  6. Ajou University School of Medicine, Republic of Korea
  7. Johns Hopkins University, United States

Abstract

Studies in rats, monkeys, and humans have found action-value signals in multiple regions of the brain. These findings suggest that action-value signals encoded in these brain structures bias choices toward higher expected rewards. However, previous estimates of action-value signals might have been inflated by serial correlations in neural activity and also by activity related to other decision variables. Here, we applied several statistical tests based on permutation and surrogate data to analyze neural activity recorded from the striatum, frontal cortex, and hippocampus. The results show that previously identified action-value signals in these brain areas cannot be entirely accounted for by concurrent serial correlations in neural activity and action value. We also found that neural activity related to action value is intermixed with signals related to other decision variables. Our findings provide strong evidence for broadly distributed neural signals related to action value throughout the brain.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Raw data to reproduce this work is archived at Dryad https://doi.org/10.5061/dryad.gtht76hj0

Article and author information

Author details

  1. Eun Ju Shin

    Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea
    Competing interests
    No competing interests declared.
  2. Yunsil Jang

    Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea
    Competing interests
    No competing interests declared.
  3. Soyoun Kim

    Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon, Republic of Korea
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1348-6401
  4. Hoseok Kim

    Neuroscience, Karolinska Institutet, Stockholm, Sweden
    Competing interests
    No competing interests declared.
  5. Xinying Cai

    Neural and Cognitive Sciences, New York University Shanghai, Shanghai, China
    Competing interests
    No competing interests declared.
  6. Hyunjung Lee

    Anatomy, Kyungpook National University School of Medicine, Daegu, Republic of Korea
    Competing interests
    No competing interests declared.
  7. Jung Hoon Sul

    Center for Synaptic Brain Dysfunctions, Institute for Basic Science, Daejeon, Republic of Korea
    Competing interests
    No competing interests declared.
  8. Sung-Hyun Lee

    Neuroscience Graduate Program, Ajou University School of Medicine, Suwon, Republic of Korea
    Competing interests
    No competing interests declared.
  9. Yeonseung Chung

    Mathematical Sciences, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea
    Competing interests
    No competing interests declared.
  10. Daeyeol Lee

    Department of Neuroscience, Johns Hopkins University, Baltimore, United States
    For correspondence
    daeyeol@jhu.edu
    Competing interests
    Daeyeol Lee, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3474-019X
  11. Min Whan Jung

    Center for Synaptic Brain Dysfunctions, Institute for Basic Science, Daejeon, Republic of Korea
    For correspondence
    mwjung@kaist.ac.kr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4145-600X

Funding

Institute for Basic Science (IBS-R002-A1)

  • Min Whan Jung

National Institute of Mental Health (DA 029330)

  • Daeyeol Lee

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Publication history

  1. Received: October 28, 2019
  2. Accepted: April 19, 2021
  3. Accepted Manuscript published: April 20, 2021 (version 1)
  4. Version of Record published: May 7, 2021 (version 2)

Copyright

© 2021, Shin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Eun Ju Shin
  2. Yunsil Jang
  3. Soyoun Kim
  4. Hoseok Kim
  5. Xinying Cai
  6. Hyunjung Lee
  7. Jung Hoon Sul
  8. Sung-Hyun Lee
  9. Yeonseung Chung
  10. Daeyeol Lee
  11. Min Whan Jung
(2021)
Robust and distributed neural representation of action values
eLife 10:e53045.
https://doi.org/10.7554/eLife.53045

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